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Arctoa (2017) 27: 49-53 doi: 10.15298/arctoa.27.05

ON THE GENUS LESKEA (LESKEACEAE, BRYOPHYTA) IN RUSSIA РОД LESKEA (LESKEACEAE, BRYOPHYTA) IN RUSSIA MICHAEL S. IGNATOV1,2, ANDREY G. BEZGODOV3, OXANA I. KUZNETSOVA2 & ELENA A. IGNATOVA1 МИХАИЛ С. ИГНАТОВ1,2, АНДРЕЙ Г. Б ЕЗГОДОВ3, ОКСАНА И. КУЗНЕЦОВА2, ЕЛЕНА А. ИГНАТОВА1

Abstract

The genus Leskea in Russia is represented by one widespread species, L. polycarpa Hedw. Records of L. gracilescens appeared to be erroneous. Analysis of nuclear ITS sequence data demonstrated that North American samples of L. gracilescens and L. obscura clearly differ from European and Asian populations in several characteristic substitutions. Anomalous morphology of plants from Yakutia and Amur Province is described and illustrated. Their distribution likely corresponds to a high and late floodings of big rivers, crossing permafrost areas.

Резюме

Род Leskea представлен в России одним широко распространенным видом , L. polycarpa Hedw. Указания на находки L. gracilescens в Амурской области были ошибочными. Анализ нуклеотидных последовательностей ядерного спейсера ITS показал, что североамериканские образцы L. gracilescens and L. obscura отличаются несколькими заменами от европейских и азиатских растений. Необычная морфология растений L. polycarpa из Амурской области и Якутии, вероятно, связана с сильными поздними паводками на больших реках, протекающих в зоне вечной мерзлоты.

KEYWORDS: Leskea, Russian Far East, Yakutia, ecomorphs

INTRODUCTION cially moss flora of China (Cao et al., 2002). In China The genus Leskea in Russia included just one species, this species was reported only recently from its NE part, L. polycarpa Hedw., in almost all publications (Abramov on the right bank of Amur River in a relatively close & Volkova, 1998; Abramova et al., 1961; Ignatov, proximity to the area where the mentioned Russian col- Afonina, Ignatova et al., 2006). Although Hedwig (1801) lection has been done. Chinese collections were reported described from Europe two species, L. polycarpa and L. as sterile (Cao et al., 2002), while in Russian specimens paludosa, the latter one was considered as a variety of sporophytes were immature, thus the sporophyte charac- the former already by authors of 19th century (e.g. ters were impossible to use. However, catenulate foliage, Schimper, 1860). Eleven infraspecific taxa within Leskea smaller stem leaves with the smaller length to width ra- polycarpa are listed in Torpicos database (http:// tio, straight and symmetric leaves, lacking characteristic www.tropicos.org/namesearch.aspx, accessed 1 May obligue apical part, and occasionally blunt apices in both 2018), but in recent checklists (Hill et al., 2006; Ros et stem and branch leaves fitted the description of L. graci- al., 2013) and Floras (Brugués & Ruiz, 2018; Redfearn, lescens. 2014) they are usually not mentioned at all. Leskea Later in Yakutia, to the north of Amur Province, we latifolia Lindb. ex Broth., described from the Caucasus collected Leskea with even more obtuse leaves, more simi- (Brotherus, 1892), was synonymized with Amblystegium lar to another American species, L. obscura. So we de- varium (Abramov, 1969). cided to test with DNA markers if the plant from Amur In the course of the flora inventory studies in the Na- Province and Yakutia really belong to L. gracillescens or ture Reserve «Norsky», Amur River basin in the Russian represent another taxon. Far East, we recently reported Leskea gracilescens (Bez- MATERIALS AND METHODS godov et al., 2013), as these plants were sufficiently dif- Sampling. In addition to L. gracillescens-like plants, ferent, agreeing in many characters with this species as we included the most common phenotypes of L. poly- it was circumscribed in moss floras of North America carpa from the Russian Far East and Yakutia into the set (Redfearn, 2014; Crum & Anderson, 1981) and espe- for sequencing, and specimen from European Russia.

1 – Lomonosov Moscow State University, Biological Faculty, Geobotany Dept., Leninskie Gory Str. 1-12, Moscow 119234 Russia – Россия, 119234, Москва, Ленинские Горы, д. 1 стр. 12, Московский государственный университет, биологический факультет, кафедра геоботаники. E-mails: [email protected] & [email protected] 2 – Tsitsin Main Botanical Garden, Russian Academy of Sciences, Botanicheskaya Str., 4, Moscow 127276 Russia – Россия 127276 Москва, Ботаническая 4, ГБС РАН. E-mail: [email protected] 3 – Joint Stock Company Kama Research Institute on Complex Deep and Superdeep Borehole Investigations, Krasnoflotskaya str., 15, Perm, 614016 Russia. – Россия 614016, Пермь, Краснофлотская, 15, АО «Камский научно-исследовательский институт комплексных исследований глубоких и сверхглубоких скважин». E-mail: [email protected] 50 M.S. IGNATOV, A.G. BEZGODOV, O.I. KUZNETSOVA & E.A. IGNATOVA

100 μm

2 3

4 2 mm 1 cm 6

7 9 8

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15 14

11 12

16 17 18

Fig. 1. Leskea polycarpa (from: Russia, Yakutia, Khangalassky Distr., 2.VIII.2016, Ignatov & Ignatova #16-160, MHA). 1, 4 – habit, dry; 2–3 – capsules; 5 – leaf transverse section; 6 – stem transverse section; 7–9 – paraphyllia; 10 – upper laminal cells; 11 – basal laminal cells; 12 – median laminal cells; 13–15 – stem leaves; 16–18 – branch leaves. Scale bars: 1 cm for 4; 2 mm for 1–3; 1 mm for 13–18; 100 μm for 5–12. On the genus Leskea in Russia 51

100 μm

9 10 2 3

12 1 8 4 11 1 mm

14 15 13 6 5 7

17 18 19

16 20 21

23 24 25

32 29 30 27 31 33 26 28 Fig. 2. 1–5 – Leskea polycarpa (1–7 from: Russia, Amursakaya Prov., 1.VII.2010, Bezgodov #34, MHA; 8–15 – from: Russia, Sakhalin, Pisarenko #0p03765, MHA); 16–21 – L. gracilescens (from: U.S.A., Ohio, Buck #50264, NY); 22–25 – L. obscura (from: U.S.A., Buck 22206, NY); 26–33 – L. cf. gracilescens (from: Russia, Amurskaya Prov., 1.VII.2010, Bezgodov #210, MHA).1, 6, 16, 22, 26, 28– upper laminal cells; 2–3, 9–10, 20–21, 32–33 – branch leaves; 5–7, 13–15, 17–19, 23–25, 29–31 – stem leaves; 4, 11–12, 27 – paraphyllia. Scale bars: 1 mm for 2–3, 5–7, 9–10, 12–15, 17–21, 23–25, 29–33; 100 μm for 1, 4, 8, 11–12, 16, 22, 26–28. 52 M.S. IGNATOV, A.G. BEZGODOV, O.I. KUZNETSOVA & E.A. IGNATOVA

Fig. 3. Five fragments of the ITS alignment of Leskea, showing characteristic substitutions indicating identity of Russian plants of different morphotypes in costrast to American specimens of L. gracilescens and L. obscura. Specimens details are in Table 1 and complete aliggnment in Supplementary materials.

Molecular protocols. acute’ in “Moss Flora of North America” (Redfearn Jr., DNA extraction and amplification were done accord- 2008); ‘acute to obtuse’ in “The moss flora of Britain ing to the laboratory protocols described in Gardiner et and Ireland” (Smith, 2004); ‘agudo o acuminado’ in al. (2005). Vouchers specimens and GenBank accession “Flora bryofítica Ibérica” (Brugués, 2018); “blunt to numbers are listed in Table 1. Sequences were aligned acute” in “Moss flora of the Middle European Russia” manually in BioEdit (Hall, 1999). (Ignatov & Ignatova, 2004). Illustrations in all these flo- RESULTS ras show slightly secund leaves with more or less ob- The molecular results are partly shown in Fig. 3, and lique apices, only rarely straight and symmetric. This complete alignment is given as a supplementary mate- character, along with differentiated stem and branch rial. There are only very few substitutions between Ameri- leaves (stem leaves being longer than wide), is consid- can samples of L. gracilescens and L. obtusa and Eur- ered as important for separating of L. polycarpa from L. asian plants, thus we present their distinction by a parts gracilescens by Redfearn Jr. (2008): L. gracilescens, con- of alignment with substitutions, instead of a tree or hap- trary to L. polycarpa, has straight leaves with symmetri- lotype network. The ITS region is found to be variable cal apices, as well as stem and branch leaves equally for separation of these three entities by characteristic sub- hardly longer than wide. stitutions. Among them, L. gracilescens and L. polycarpa Most Leskea specimens from Russia fully agree with lack infraspecific variation in these positions, and L. the mentioned features of L. polycarpa, except for the obtusa has one vatiable position. anomalous specimen from Amurskaya Province referred Specimens from the Amur Province, as well as from previously to L. gracilescens. In Fig. 2: 1–15, two speci- Yakutia revealed no differences in sequences from specimens of L. polycarpa from Asian Russia are shown, with mens of the common phenotypes of L. polycarpa, both clearly asymmetrical stem leaves, oblique leaf apices and from the Far Eastern and European populations (Fig. 3). less oblong branch leaves with obtuse apices. However, specimen from Amurskaya Province (Fig. 2: 26–33) re- DISCUSSION sembles L. gracilescens from North America (Fig. 2: 16– Although the present study results in no taxonomic 21) rather than L. polycarpa in shape of stem and branch novelties, the fact of such extreme variation is worthy leaves, which are straight and have symmetrical apices. describing and illustrating (Figs. 1–2). Obviously, the Nevertheless, evidence from molecular markers suggests record of L. gracilescens from Russia and probably also that this deceiving resemblance is likely caused by the from China are based on the ecomorphs of L. polycarpa. influence of ecological conditions. Leaf apices in L. polycarpa are described as ‘blunt or Another peculiar specimen with all leaves obtuse, even

Table 1. Specimens of the genus Leskea used in molecular study, with GenBank accession numbers. Species Specimen Isolate Genbank number L. gracilescens USA: Connecticut, coll. Tan #91502 (MHA) OK555 MH558262 L. gracilescens USA: Chicago, 6.X.2013 Ignatov (MHA) OK556 MH558263 L. gracilescens USA: New York, Buck 57814 (NY barcode 1221900) OK541 MH558264 L. obtusa USA: New Jersey, Buck 22206 (NY barcode 489277) OK545 MH558265 L. obtusa USA: Missouri, Buck 30103 (NY barcode 489398) OK544 MH558266 L. obtusa USA: Kansas, Buck 46377(NY barcode 680473) OK542 MH558267 L. polycarpa Russia: Amurskaya Province, 1.VII.2010 #69 (MHA) OK428 MH558268 L. polycarpa Russia: Ryazan, 11.XI.2009 Donskov (MHA) OK551 MH558269 L. polycarpa Russia: Amurskaya Province, 1.VII.2010 Bezgodov #34 (MHA) OK552 MH558270 L. polycarpa Russia: Vladivostok, Ignatov #08-355a (MHA) OK553 MH558271 L. polycarpa Russia: Sakhalin, Pisarenko #3765 (MHA) OK554 MH558272 L. polycarpa Russia: Yakutia, Ignatov & Ignatova 16-160 (MHA) OK1438 MH558273 On the genus Leskea in Russia 53 with rounded apices, was collected in Central Yakutia. CRUM, H. A. & L. E. ANDERSON. 1981. Mosses of the Eastern North However, its stem leaves are more longer than wide in America. Vol. 2. – Columbia University Press, New York. pp. 664– 1328. comparison with branch leaves and have slightly oblique CAO, T., J. SUN & C. GAO. 2002. Leskeaceae. – In: Wu, P-c. & M. apices (Fig. 2), which is in agreement with circumscrip- Crosby (eds.) Moss flora of China, English version. Vol. 6. Hookeri- tion of L. polycarpa according to Redfearn Jr. (2008). aceae–Thuidiaceae, Science press (Beijing & New York) & Missouri Capsules in this specimen are also slightly different from Botanical Garden Press, pp. 99–130. common morphotype of L. polycarpa, being straight and GARDINER, A., M. IGNATOV, S. HUTTUNEN & A. TROITSKY. 2005. shorter than usual. However, molecular markers did not On resurrection of the families Pseudoleskeaceae Schimp. and Pylaisi- reveal any difference between this specimen and other aceae Schimp. (Musci, Hypnales). – Taxon 54: 651–663. specimens of L. polycarpa, pointing on wider morpho- HALL, T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. – Nucleic logical variability of this species in peculiar ecological Acids Symposium Series 41: 95–98. conditions in permafrost areas of Asian Russia with re- HEDWIG, J. 1801. Species Muscorum Frondosorum. – Lipsiae. 352 pp. peated strong summer floods caused by the permafrost HILL, M. O., N. BELL, M. A. BRUGGEMAN-NANNENGA, M. BRU- melting. GUÉS, M. J. CANO, J. ENROTH, K. I. FLATBERG, J.-P. FRAHM, M. T. GALLEGO, R. GARILLETI, J. GUERRA, L. HEDENÄS, D. T. ACKNOWLEDGEMENTS HOLYOAK, J. HYVÖNEN, M. G. IGNATOV, F. LARA, V. MAZIM- The work was supported by RSF (grant no. 18-14- PAKA, J. MUŃOZ & L. SÖDERSTRÖM. 2006. An annotated check- 00121). list of the mosses of Europe and Macaronesia. – Journal of Bryology 28: 198–267. LITERATURE CITED IGNATOV, M. S., O. M. AFONINA & E. A. 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